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SQUAMATA: SCINCIDAE) Acta Zoológica Mexicana (Nueva Serie), Vol Acta Zoológica Mexicana (nueva serie) ISSN: 0065-1737 [email protected] Instituto de Ecología, A.C. México JEREZ, ADRIANA; SÁNCHEZ-MARTÍNEZ, PAOLA MARÍA; GUERRA-FUENTES, RICARDO ARTURO EMBRYONIC SKULL DEVELOPMENT IN THE NEOTROPICAL VIVIPAROUS SKINK MABUYA (SQUAMATA: SCINCIDAE) Acta Zoológica Mexicana (nueva serie), vol. 31, núm. 3, diciembre, 2015, pp. 391-402 Instituto de Ecología, A.C. Xalapa, México Available in: http://www.redalyc.org/articulo.oa?id=57542699005 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative ActaISSN Zool. 0065-1737 Mex. (n.s.) 31(3) (2015) Acta Zoológica Mexicana (n.s.), 31(3): 391-402 (2015)391 EMBRYONIC SKULL DEVELOPMENT IN THE NEOTROPICAL VIVIPAROUS SKINK MABUYA (SQUAMATA: SCINCIDAE) A JEREZ1, P M SÁNCHEZ-MARTÍNEZ2 & R A GUERRA-FUENTES2,3 1Departamento de Biología. Universidad Nacional de Colombia, Sede Bogotá, Bogotá, Colombia. Carrera 45 No 26-85, Bogotá, Cundinamarca, Colombia. <[email protected]> 2Museu de Zoologia da Universidade de São Paulo, São Paulo, Brasil. Av. Nazaré 481, Ipiranga, 04263-000, São Paulo (SP), Brasil. <[email protected]>; 3<[email protected]> Recibido: 01/03/2015; aceptado: 09/10/2015 Jerez, A., Sánchez-Martínez, P. M. & Guerra-Fuentes, R. A. 2015. Jerez, A., Sánchez-Martínez, P. M. & Guerra-Fuentes, R. A. 2015. Embryonic skull development in the neotropical viviparous skink Desarrollo embrionario del cráneo en la lagartija vivípara Mabu- Mabuya (Squamata: Scincidae). Acta Zoológica Mexicana (n.s.), ya (Squamata: Scincidae). Acta Zoológica Mexicana (n.s.), 31(3): 31(3): 391-402. 391-402. ABSTRACT. The systematics of the Americans skinks of the genus RESUMEN. La sistemática del género Mabuya ha sido extensamente Mabuya have been extensively studied, with new arrangements based estudiada en América y se han propuesto varios arreglos taxonómicos on molecular analysis. However, the skeletal morphology, their de- con base en análisis moleculares. Sin embargo, aspectos relacionados velopment and ontogenetic variation have been poorly studied in this con la morfología del esqueleto, su desarrollo y variación ontogenéti- genus. We described the embryonic skull development of three species ca han sido probrementente estudiados en este género. En el presente of Mabuya and compare it with the African species Trachylepis cap- trabajo se describe el desarrollo embrionario del cráneo en tres espe- ensis. We observed that American genus Mabuya presents differences cies del género Mabuya y se compara con el de la especie africana in the skull development, including the pila antotica, orbitosphenoid, Trachylepis capensis. Se encontró que el género Mabuya presenta di- vomer, and the basicranial fenestra closure. These morphological dif- ferencias en el desarrollo del cráneo respecto a la especie africana, ferences in Mabuya species may be interpreted as putative synapomor- incluyendo la pila antótica, el orbitosfenoides, el vómer, y el cierre de phic characters. la fenestra basicraneal. Estas diferencias en el desarrollo del cráneo Key words: Skull development, chondrocranium, Mabuya, skin, Scin- son importantes, ya que su presencia en todo el género Mabuya sugiere cidae, Squamata que se podría tratar de sinapomorfias para este clado. Palabras clave: Desarrollo craneal, condrocráneo, Mabuya, Scinci- dae, Squamata INTRODUCTION posal and all species in this work are regarded to the ge- nus Mabuya. The genus Mabuya constitutes a monophyletic unit with a All Mabuya species present viviparous reproduction, recent diversification, and exhibits a unique combination smooth scales, lower eyelid with a semi-transparent disc, of reproductive features in Squamata (Blackburn & Vitt pterygoid teeth absent, and 25-31 presacral vertebrae 1992; Mausfeld et al. 2002; Carranza & Arnold 2003; (Mausfeld et al. 2002). This genus inhabits mainly low- Whiting et al. 2006; Miralles & Carranza 2010). land forests and evolved with a group of specializations Until recently, the pantropical genus Mabuya includ- related to viviparity, which are unique among reptiles and ed more than a hundred species distributed in America, convergent only with placental mammals: a long period Africa and Asia (Greer & Nussbaum 2000; Greer et al. of gestation (9 to 12 months) and microlecithal eggs (0.9- 2000). However, on the basis of a molecular phylogenetic 2.2 mm) with a highly placentotrophic nutritional pat- analysis this genus was divided into four clades (Maus- tern (Blackburn & Vitt 1992; Blackburn 1993; Jerez & feld et al. 2002). In this way, the genus Mabuya actually Ramírez 2001, 2003). includes about 53 species, distributed from Mexico to Ar- Despite the recent phylogenetic and taxonomic in- gentina (Ávila-Pires 1995; Mausfeld et al. 2002; Miralles terest in the evolution of the genus Mabuya (Mausfeld et al. 2005). The other three clades are Trachylepis (Fitz- et al. 2002; Carranza & Arnold 2003; Jesus et al. 2005; inger 1843) in Africa, Chioninia (Gray 1845) in Cape Miralles et al. 2005; Whiting et al. 2006; Miralles et al. Verde, and Eutropis (Fitzinger 1843) in Asia (Mausfeld 2009; Miralles & Carranza 2010; Hedges & Conn 2012), et al. 2002; Bauer 2003). We follow this taxonomic pro- osteological and ontogenetic descriptions in comparative 392 Jerez et al.: Skull development in Mabuya studies are scarce. Regarding African species, Skinner Mabuya sp. was compared with that of M. cassaira and (1973) described the ontogenetic and adult morphology in M. macrorhyncha, two Brazilian species. We described Trachylepis capensis skull, whereas Rao & Ramaswami a series of eight embryos of M. cassaira from Bertioga, (1952) described the fully formed chondrocranium and SP Brazil (MZUSP-40720, MZUSP-40771, MZUSP- the adult osteocranium of the Asian Eutropis carinata. 40777, MZUSP-40779, MZUSP-45703), and five of M. Concerning American species, Jerez (2012) described the macrorhyncha from Guarujá, SP, Brazil (MZUSP-40695, adult skull of Colombian Andean population of Mabuya MZUSP-40792, MZUSP 40800) and Ilha dos Búzios, SP, sp., and Caicedo (2012) analyzed the adult skull in differ- Brazil (MZUSP-11148, MZUSP 11176). In this compari- ent species and populations in Colombia. son we described embryos of stages 32, 39 and 40 (D&H) Hence, the main purpose of this work is to describe the for all species. The stage 34 (D&H) is described just for development of the embryonic skull in Mabuya sp., M. Mabuya sp. The skeletal embryonic development was cassaira and M. macrorhyncha. In addition, the chondro- described using cleared and double-stained specimens, cranium of Mabuya is compared with the species of the prepared following Wassersug (1976). The description of old world Trachylepis capensis and Eutropis carinata, the chondrocranium follows those of Bellairs & Kamal therefore, these morphological studies could provide ad- (1981). In Mabuya sp. the first stage is described, while ditional anatomical characters to support the taxonomic in the subsequent stages only the registered variations are status of this American clade as monophyletic. This is explained. In contrast, with M. caissara and M. macro- particularly important, given that Hedges & Conn (2012) rhyncha only the differences relating to Mabuya sp. are proposed sixteen genera for America. On the other hand, reported. though many molecular phylogenetic analyses support the monophyly of American clade (Mausfeld et al. 2002; Carranza & Arnold 2003; Jesus et al. 2005; Whiting et RESULTS al. 2006; Miralles & Carranza 2010), some herpetologists consider that the division of pantropical genus Mabuya in Mabuya sp. Stage 32-33 (Fig. 1): In this stage, elements four genera has been premature (Jesus et al. 2005; Whit- of three regions of the chondrocranium are observed: the ing et al. 2006). anterior ethmoidal region, the intermediate orbitotempo- ral region, and the posterior occipital region (Table 1). In the ethmoidal region, the cartilages of the nasal capsule MATERIALS AND METHODS start being condensed. The interorbital septum is low and contacts the trabecula communis. In the posterior region, We described the skull development in an Andean popu- the skull consists of the basal plate and the occipital arch. lation of Mabuya sp. and compared it with the transan- The elements of splachnocranium, the quadrate, the as- dean species M. caissara and M. macrorhycha. Mabuya is cending process and the Meckel´s cartilage are observed widely distributed in Colombia (Sánchez et al. 1995) and their populations represent a complex of species (Ávila- Pires 1995; Miralles et al. 2005; Miralles 2006). According to Miralles (2005) neither M. mabouya nor M. nigropunc- tata, nominations for populations in Colombia, are pres- ent in the Andean Colombian regions. For this reason, in this work the studied population is referred as Mabuya sp. The embryos of Mabuya sp. were taken from females of a population collected at the Inspección de Policía Guadu- alito, in the Municipality of Yacopí, Cundinamarca, Co- lombia. They are housed in the Colección Herpetologica, Escuela de Biología, Universidad Industrial de Santander. A series of twelve embryos of Mabuya sp. was selected (UIS-R-289, 310, 311, 314, 319, 320, 321, 351, 355, 366, 404, and 415). Stages of development follow Defaure & Hubert (1961), this table starts at stage 1 with the cleav- Figure 1. Chondrocranium
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